Download 2a di cop. e pag. 3 - Ornitologia Siciliana

Massa imp.
25-11-2006
12:21
Pagina 5
Avocetta 30: 5-14 (2006)
Biological significance and conservation of biogeographical
bird populations as shown by selected Mediterranean species
BRUNO MASSA
Stazione Inanellamento, c/o Dipartimento SENFIMIZO dell’Università di Palermo, v.le delle Scienze 13, I-90128 Palermo,
Italy ([email protected])
Abstract – From the conservation point of view there is an important difference between species that are treated as whole and species
considered as separate subspecies; these represent important components of biodiversity and deserve conservation for their potential evolution and their characteristics. EU Bird Directive shows an attempt to protect subspecific taxa, when really necessary for conservation
purposes. There are some examples of species regarded as secure, if considered as whole, that turn out to be endangered or critically
endangered when treated as subspecies (e.g. Mediterranean storm petrel, lanner falcon, rock partridge, Andalusian hemipode, long-tailed tit and crossbill). Status of some species should have to be modified, basing information on more objective comparison with those
available for related species (e.g. the pairs Manx and Yelkouan shearwaters, European and spotless starling, and North African blue tit).
Moreover, some species have a very restricted distribution, that might be considered an endemic bird area, holding two or more species
with a range covering less than 50,000 km2 (e.g.: Marmora’s warbler, Cyprus warbler, Cyprus wheatear and Corsican citril finch). Here
I suggest to reconsider, among future conservation priorities, the status of a number of S European species in the light of previous considerations, avoiding some paradoxes, such as incongruity of risk level, when compared to other bird species.
Riassunto – Significato biologico e conservazione di popolazioni biogeografiche di alcune specie dell’avifauna mediterranea. In tema
di conservazione della natura, c’è una sostanziale differenza se una specie è trattata nel suo complesso o si prendono in considerazione
separatamente le sue sottospecie; queste ultime rappresentano componenti molto importanti della biodiversità e meritano un’adeguata
conservazione per l’intrinseco potenziale evolutivo e le loro caratteristiche uniche. L’Allegato I della Direttiva Uccelli (409/79 e 244/91)
è indubbiamente un fondamentale tentativo a livello europeo di tutelare taxa sottospecifici, nei casi in cui per essi si ritengono necessarie
azioni di conservazione. Tuttavia, queste indicazioni non sono state seguite in importanti occasioni; ci sono numerosi esempi di specie
definite “sicure” se considerate nel loro complesso, ma che risultano “minacciate” o “minacciate in modo critico” se trattate a livello sottospecifico (esempi sono l’uccello delle tempeste mediterraneo, il lanario, la coturnice, la quaglia tridattila, il codibugnolo ed il crociere).
Lo status di alcune specie dovrebbe essere corretto, sulla base di informazioni più obiettivamente confrontate con quelle disponibili di
specie affini (ad esempio le coppie berta minore atlantica/berta minore mediterranea, storno/storno nero e la cinciarella algerina). Inoltre,
esistono specie con una distribuzione molto circoscritta, che andrebbe correttamente considerata come un’area avifaunistica endemica,
cioè ospitante due o più specie con un areale inferiore ai 50.000 km2 (esempi sono la magnanina sarda, la silvia di Cipro, la monachella
di Cipro ed il venturone corso). Alla luce delle considerazioni fatte, si propone, tra le priorità conservazionistiche dell’immediato futuro,
di riconsiderare lo status di molte specie europee, evitando in tal modo alcuni paradossi, quale l’incongruità del livello di rischio per
molte specie d’uccelli, se paragonata ad altre.
Biodiversity is the total variety of life on Earth,
including all genes, species and ecosystems and the
ecological processes of which they are part (Wilson
1988, Mc Neely et al. 1990); maintaining it means
preserving species on the whole, and their isolated
subspecies as well. Conservation is a science which
clearly needs to dialogue with bureaucracy and politics. Investigations on species’ status and list perReceived 10 April 2006, accepted 26 September 2006
Assistant editor: D. Rubolini
© 2006 CISO – Centro Italiano Studi Ornitologici
centages of declining species clearly represent an
important information, but it is necessary to avoid
ambiguity in preserving species and habitats. Many
European researchers gathered their efforts in a
foundamental work, largely based on IUCN (2004)
criteria, that concerns the new update of status and
trend of European bird populations (BirdLife International 2004). Novelty generally brings both opportunities and risks. Since this update represents a scientific source, the main opportunity is that its contents are likely to be used as the main reference for
5
Massa imp.
25-11-2006
12:21
Pagina 6
Massa
the update of Annex I of Bird Directive 409/79.
However, information sources on population estimates and trends provided by different countries are
heterogeneous and have a variable quality; this
entailed some subjective choices in the inclusion of
species within the different categories. Some threatened species could run the risk not to obtain the necessary attention at European level. The aim of
BirdLife International (2004) is the identification of
priority species so that conservation actions can be
taken to improve their status; therefore the exclusion
of some species/subspecies from its official list
would mean also their exclusion from conservation
processes. Of course I agree with the IUCN (2004)
criteria for the red list compilation, but I believe that
the right moment has come to schedule, among
future priorities for bird conservation, the inclusion
of some biogeographical populations which are the
result of an evolutionary process in progress. EU
Bird Directive (709/79 and 244/91, Appendix I)
shows an attempt to consider subspecific taxa, when
really necessary for conservation purposes (e.g.:
Phalacrocorax aristotelis desmarestii, Lagopus
muta helvetica, Alectoris graeca whitakeri, Alectoris
graeca saxatilis, Perdix perdix italica, Perdix perdix
hispaniensis, etc.). These should be preserved for
their potential evolution and acquisition of unique
characteristics, which represent important components of biological diversity; if effectively isolated,
they may become new species by acquiring genetic
isolating mechanisms. Bird subspecies are allopatric
subpopulations, generally maintained by spatial segregation, that share i) a unique geographic range or
habitat, ii) a group of phylogenetically concordant
array of phenotypic and genetic characters, iii) a
unique natural history relative to other subdivisions
of the species, (still) genetically compatible with
other subpopulations (O’Brien and Mayr 1991,
Amadon and Short 1992).
Each of the geographical forms classed as subspecies occupies particular areas which, all together,
give the range of the species as a whole. If these geographical forms were classed as allospecies (populations derived from the same common ancestor whose
ranges differ and do not touch), we would have several smaller ranges in place of a large one (Newton
2003). From the conservation point of view there is
an important difference to treat a species as whole or
its subspecies separately. Taxa that are apparently
well differentiated, possibly young or having frequent gene flow with other subspecies, still do not
6
reach the reproductive isolation in many populations.
Sometimes results of molecular genetics contradict
previous ideas about species integrity or taxonomic
distinctions based on phenotypic descriptions; an
interesting example is the pair F. peregrinus/F. pelegrinoides (Wink and Sauer-Gürth 1998) treated as
separated species by some authors; nevertheless,
even if recent molecular researches (Seibold et al.
1993, Wink and Seibold 1996) concluded that pelegrinoides is a valid species, very close to peregrinus,
Wink et al. (1998), using mtDNA cytochrome b
sequence, found a very high affinity between peregrinus and pelegrinoides with a genetic distance
below 0.6% (distance at specific level in Falconidae
family should be over 1.5%), proposing to continue
to treat them as conspecific. Another interesting
example concerns the sparrows; Hagemeijer and
Blair (1997) list the Italian sparrow (Passer italiae)
as a stabilized hybrid, while the authors of BirdLife
International (2004) neglect it and misunderstand
that the very small figure of 50-100,000 pairs of
Passer domesticus (living only on the Alps) is the
total Italian amount (thus excluding the much larger
“italiae” population). If the subspecies level should
get an appropriate acknowledgement, it could enter
into official lists, when conservation status of these
“subgroups” requires particular attention. The continuity of the evolutionary process through space and
time means that decisions on the limits of species and
their distributional boundaries are, to some extent,
arbitrary, but the way in which species are defined
and delineated can influence our perception of distribution patterns and diversity (Newton 2003). Assuming that a decision to treat a taxon at species or subspecies level may depend on the scientist subjectivity, on the species concept applied (Rojas 1992, de
Queiroz 1998, Fraser and Bernatchez 2001, Helbig et
al. 2002) or on methodology used (Pasquet and
Thibault 1997, Haring et al. 1999, Sangster 2000,
Sangster et al. 2005), a careful use of subspecies level in global approaches may result more useful and
suitable for bird conservation.
Conservation biologists tried to search for methods distinguishing unambiguous units for conservation purposes, and employed evolutionarily significant units (ESU) as basic units of analysis, when evidence clearly indicated that a formally recognized
species either fails to convey important evolutionary
and geographical information or fails in delineating
a natural entity (Riddle and Hafner 1999). “ESU”
was coined by Ryder (1986) as “a subset of the more
Massa imp.
25-11-2006
12:21
Pagina 7
Conservation and Mediterranean species
inclusive entity species, which possess genetic
attributes significant for the present and the future
generations of the species in question”; interestingly,
ESU had both important and biological employ
under the USA Endangered Species Act, the Australian Environment Protection and Biodiversity
Conservation and the Canadian Species at Risk Act.
Entities defined as ESU arise from the accumulation
of genetic differences through the various roles of
evolutionary forces through the time. However,
along the years ESU concept varied very much in
accordance with different criteria (e.g. Fraser and
Bernatchez (2001) report eight different definitions);
the lack of agreement about the concept of the ESU
origins from the same philosophical and interpretative dilemmas that plague the scientific definition of
species (Kelt and Brown 2000, Green 2005). Consequently, as well as the species concept, no definitive
concept of ESU prevailed so far. Moreover, Crandall
et al. (2000) proposed that ESU concepts might be
replaced by a more holistic concept of species, consisting of populations with varying levels of gene
flow evolving through drift and selection. Finally,
Green (2005) proposed the use of the Designatable
Units (DU), methodology adopted by the Committee
on the status of Endangered Wildlife in Canada;
determining DUs constitutes a two-part test and
asks, in the first place, if putative DUs are distinguishable and, then, if they have different conservation status; DUs may also be identified on the basis
of demonstrations of genetic distinctiveness, similar
to those used for the recognition of the ESU (Green
2005). Species ranges are genetically, demographically, spatially, and ecologically so heterogeneous
that current taxonomy cannot always capture whole
relationships, but measures to prevent the reduction
or the loss of the species should not be postponed for
a lack of full scientific certainty. Overall, considering species as dynamic evolutionary units is less
affected by the species problem and more related to
conservation science (Rojas 1992).
In the last 10-20 years some species have undergone numerical and distributional range increases
(e.g.: Columba palumbus, Turdus merula, Sylvia atricapilla, Sylvia melanocephala, Regulus ignicapilla,
Certhia brachydactyla, Fringilla coelebs, Carduelis
chloris, Emberiza cirlus, etc.); thus, because of their
well documented and justified secure status, it seems
reasonable to transfer them from the category of
species with favourable conservation status, but concentrated in Europe, to “secure” category (BirdLife
International 2004). Others show a scattered distribution clearly divided according to subpopulations,
characterized by biological, morphological and genetic traits that allow to consider them independently.
Habitat loss and fragmentation is considered by far
the most pervasive threat, impacting 86% of endangered birds; over-exploitation and invasive alien
species are also impacting about 30% of threatened
birds (the latter 67% on islands) (Baillie et al. 2004);
in addition, an evident difference exists between biological cycles of migrant and sedentary birds, since
the density of the first is consistently influenced by
conditions in different parts of the world. Small areas,
such as Mediterranean islands, host many endemic
taxa, among birds too; even if threatening processes
vary both within and between taxonomic groups,
threats to terrestrial and marine birds in these fragile
ecological systems need conservation interventions to
ensure their continued survival.
Hereby I report some examples of biogeographical populations that should benefit of a stricter conservation approach.
BIOGEOGRAPHICAL RELEVANCE OF PRESERVING SUBSPECIES
Cory’s shearwater Calonectris diomedea
Assuming that C. edwardsii is a valid species
(Hazevoet 1995), currently at least three large populations of C. diomedea are known, belonging to two
subspecies, namely C. d. borealis (Atlantic islands,
wintering in S America) and C. d. diomedea, with
two populations, that differ biometrically (Massa and
Lo Valvo 1986) and in their vocalizations (Bretagnolle and Lequette 1990), one in the central-western
Mediterranean, wintering in S Africa, and the other in
the eastern Mediterranean. According to Randi et al.
(1989) and Wink et al. (1993) genetic differences
between birds in Mediterranean and Atlantic colonies
are of the same order generally found between subspecies, showing a moderate gene flow in Mediterranean and Atlantic C. diomedea. The high nest site
fidelity (Jouanin et al. 1977, Massa and Lo Valvo
1986, Ristow et al. 1990, Thibault 1993, 1994,
Swatschek et al. 1994) minimizes the immigration
contribution of external individuals to the dynamics
of each colony (but cf. Lo Valvo and Massa (1988)
and Thibault and Bretagnolle (1998), who record
interesting evidence of gene flow between the two
7
Massa imp.
25-11-2006
12:21
Pagina 8
Massa
subspecies). Different populations of Atlantic and
Mediterranean Calonectris diomedea differ in mtDNA cytochrome b sequence as much as 1.51-1.87 %;
it should be reminded the fact that between taxa
recently raised to species level, Larus cachinnans, L.
fuscus and L. argentatus, mtDNA cytochrome b
divergence is 0.69-2.04 % (Helbig 1994). According
to BirdLife International (2004) the populations of C.
diomedea amount to 270-290,000 pairs, have a vulnerable status and are in decline. As other shearwaters, they show strong philopatry, with the majority of
young returning to the colony where they hatched,
and a very small demographic growth (e.g.: Ristow et
al. 1990). It is evident that all three biogeographical
populations need to be preserved. Additionally, some
populations undergo an anachronistic and illegal
over-exploitation of eggs and more recently the rat
predation; for instance, people of Linosa Is. (Sicilian
Channel, Italy) every year collect approximately 23,000 eggs from a population of about 10,000 pairs,
and in the last years rats are a further reason of their
low breeding success. BirdLife International (2004)
includes the species among the SPEC2 category
(with unfavourable conservation status, concentrated
in Europe). In this case, even separating the three biogeographical populations cited above, they would
remain in the SPEC2 category.
European and Mediterranean storm petrel Hydrobates pelagicus
As the other petrels, this is a k-selected species,
showing a very high breeding site fidelity (Amengual
et al. 1999, Lo Valvo and Massa 2000). Extinction
probability should be higher for species with low
intrinsic rates of increase, compared to r-selected
species, when population is small (Pimm et al. 1988).
Additionally, two biometrically and genetically distinct subspecies have been recorded, one (H. p.
pelagicus) in the Atlantic, and the other (H. p.
melitensis) in the Mediterranean, the latter characterized by a larger size and some different reproductive
parameters (Hemery and D’Elbée 1985, Catalisano et
al. 1988, Bretagnolle 1992, Lo Valvo and Massa
2000, Lalanne et al. 2001). Divergence between
pelagicus and melitensis possibly resulted from paleogeographic changes in the Strait of Gibraltar, making isolation of the Mediterranean population possible. The latter, indeed, shows a very low genetic differentiation, unlike the Atlantic population (Cagnon
8
et al. 2004). In total, Mediterranean basin hosts
8,500-15,200 pairs of melitensis, a very small proportion of the whole European population, estimated
between 430,000 and 510,000 pairs (BirdLife International 2004). A major factor limiting the breeding
distribution of this species is the presence of safe
colony sites on islands, that is why the Mediterranean
populations are so depleted. Tucker and Heath (1994)
considered the species as localized (= with populations highly concentrated in few sites), while
BirdLife International (2004) changed the status to
secure, thanks to improved knowledge of the Atlantic
distribution and numbers, which show a stable trend.
From the conservation point of view, it should be a
prerequisite condition to treat melitensis separately,
maintaining it in the SPEC2 category; Mediterranean
populations, indeed, are declining and critically
threatened in their breeding sites, due to human
impact and rat predation (Massa and Sultana 1991).
Lanner falcon Falco biarmicus
Its global European population is estimated as much
as 480-900 pairs, the majority of which lives in
Turkey and Italy. If we consider the species as
whole, Europe holds a tiny proportion of the global
range. As regards its subspecific status, it is clearly
differentiated in morphologically distinguishable
isolated populations, breeding in S Europe and small
part of Middle East (Falco b. feldeggii), in N Africa
(F. b. erlangeri), and in Africa, S of Sahara (F. b.
biarmicus). In Europe the species is considered
SPEC3, vulnerable (BirdLife International 2004);
for conservation purposes, it should be more consistent to consider these sedentary biogeographical
populations, among which apparently there is no
gene flow, as separated taxa and to include the “rare”
European subspecies within the SPEC2 category.
Rock partridge Alectoris graeca
It is one of three Mediterranean endemic species of
the genus Alectoris; endemic to Alps, Apennines,
Balkans and Sicily, it has undergone a continuing
decline over the last decades, mainly due to hunting.
Listed as SPEC2 by Tucker and Heath (1994) and
BirdLife International (2004), it is subdivided into
populations, fairly distinguishable and described as
distinct subspecies. Genetic data partially support
Massa imp.
25-11-2006
12:21
Pagina 9
Conservation and Mediterranean species
subspecies subdivisions, and allow to delimite distinct
conservation units. According to Lucchini and Randi
(1998) and Randi et al. (2003), populations from
Apennines and Balkans were probably connected by
gene flow since the last glacial maximum, through a
late Pleistocene Adriatic landbridge, while estimates
of divergence times suggested that Sicilian rock partridges were isolated for more than 200,000 years.
Deglaciated Alps were probably colonized by two distinct source populations, bringing about differences
observed between eastern and western populations.
Rock partridges in Sicily, formally recognized as A. g.
whitakeri, met the criteria for a distinct evolutionary
significant unit; Randi et al. (2003) identified two
major mtDNA phylogroups, splitting partridges from
Sicily vs. all the other sampled populations at an average genetic distance of 0.035, corresponding to 65%
of the average distance between closely related
species of Alectoris. Interestingly, bottleneck and mismatch analyses indicate that rock partridges lost variability through past population declines, and did not
expand recently. Assuming the uniqueness of this taxon, very declining and critically endangered in the
few Sicilian sites where scanty populations still survive, on an area certainly smaller than 5,000 km2, it
should be more consistent to treat this subspecies separately from the others, listing it within the SPEC1
category (species of global conservation concern).
Noteworthy is that the Bird Directive lists A. g.
whitakeri and A. g. saxatilis in the Annex I.
Andalusian hemipode Turnix sylvaticus
Almost certainly it has become extinct in Europe,
and it is on verge of extinction in N Africa. Violani
and Massa (1993) found remarkable biometrical differences between the Mediterranean form (T. s. sylvaticus) and sub-Saharan and asiatic ones, concluding that its extinction does mean the disappearance
of a Mediterranean endemism for ever; following
them, Mediterranean subspecies should be included
in the SPEC1 category, not SPEC3, as BirdLife
International (2004) did.
Long-tailed tit Aegithalos caudatus
Widespread and common species everywhere in
Europe, where global populations cover less than half
of its global distribution. Consequently its status is
considered secure in the NonSPECE category (BirdLife International 2004). However, there are some
geographically isolated populations, whose subspecific status is clearly recognized (e.g. A. c. siculus in
Sicily); their sedentary habits and probable absence
of gene flow with other populations should bring
conservation scientists to treat them separately.
European and Mediterranean crossbills Loxia
curvirostra
Variability in the cone crop of coniferous trees is
thought to be the most important cause of the
nomadic nature of this species; nevertheless, nomadism did not prevent the isolation of geographical
forms. This species is a very interesting example of
evolutionary process in progress. Crossbills with a
slender bill feed on several conifer species, whereas
those with a strong bill feed only on pines, which
have cones larger than other conifers. Correlation
between cone scales length and the index of bill curvature supports the hypothesis that bill size is an
adaptive character for feeding on pine cones (Lavauden 1924, Massa 1987, Knox 1990, Clouet 2003).
Fossils prove that L. curvirostra was definitely present in S Europe and the Near East at least from the
middle Würmian onwards and probably throughout
the Würmian, and that larger birds (L. pytyopsittacus
size) existed at least in a limited area of the W Alps
from the glacial maximum onwards; S European
crossbills were isolated from their Siberian congeners during the early and middle Würmian (Tyrberg 1991). Large-billed crossbills on Mediterranean
islands and N Africa are probably descendants of
Pleistocene populations living on dominant conifers.
They must have fed mainly on pine cones, since other conifers were absent or rare W of Urals. A centrifugal spread from central European populations
northwards and southwards may have produced
large-billed forms (Eck 1981), such as L. scotica, L.
pytyopsittacus and Mediterranean populations; feeding on pines and evolving relatively long tongues
which increased probing ability (Benkman 1987) on
exploiting conifers regularly fruiting for extended
periods, they acquired the potential to become sedentary (Massa 1987, Senar et al. 1993, Clouet and
Joachim 1996, Clouet 2003). From analysis of mtDNA, species formation in birds is estimated to take
around 2.5 million years, varying between 0.2 and
5.5 million years, while subspeciation is estimated to
9
Massa imp.
25-11-2006
12:21
Pagina 10
Massa
take a short time, sometimes less than 10,000 years
(Newton 2003); it is not certain that an isolation period of c. 10,000 years is sufficient for speciation to
take place. The three taxa of Crossbills (Loxia curvirostra, L. scotica and L. pytyopsittacus) show no consistent differences in either mithocondrial DNA or
nuclear microsatellite sequences, and substantial
overlap in the main morphological character (bill
depth) that supposedly separates them (Piertney et al.
2001). They occur as different ecotypes, differing in
body size, call notes, bill size, colours and food preferences. Selective pressures were sufficiently strong
to trigger and enhance morphological evolution and
rapid local adaptation to resources, without necessarily promoting the development of reproductive barriers between morphs (Questiau et al. 1999). Following Groth (1993), N American crossbills belong to
eight sibling species, where mated pairs contain
members of the same morphotype in areas where different forms are sympatric. European crossbills possibly belong to different species as well, even if it is
currently not clear how these forms avoid interbreeding in the wild (see Knox 1990 for L. scotica).
Mediterranean populations consist of small flocks,
generally of tens, rarely of hundreds, so local, sedentary and strictly linked to pine forests that may be
considered as endemic taxa; consequently, their status is never secure and deserves a particular attention.
ADJUSTMENT OF THE STATUS OF SOME
SPECIES
Yelkouan shearwater Puffinus yelkouan
Assuming that P. mauretanicus is a separate species
(Heidrich et al. 2000), Europe holds 13-33,000 pairs
on a geographic range of about 100,000 km2 (almost
exclusively on islands), representing more than 95%
of the whole population. Although data about trends
during 1990-2000 were not available for certain
countries (4 out of 9, that is 45%) and only four
countries considered this species stable, Tucker and
Heath (1994) and BirdLife International (2004)
record it as stable and with secure status (respectively including it in SPEC4 and NonSPECE categories,
that is with favourable conservation status, but concentrated in Europe). However, the whole population of this species is very small and scattered on
islets (differently from the SPEC2 P. puffinus and C.
diomedea, large colonies are rare in P. yelkouan) and
10
no new nesting colony has been recorded (differently from P. puffinus, which has established since 1977
on a N American island off Newfoundland, far from
any other known colony: Storey and Lien 1985).
From the conservation point of view, the place of P.
yelkouan should have been more correctly within
SPEC2, with vulnerable status.
European starling Sturnus vulgaris and spotless
starling Sturnus unicolor
The first is a widespread breeder across most of
Europe, where less than half of its global population
lives; it has been introduced in S Africa (1897), Australasia (1856-1881) and N America (1844-1890),
where currently it has a population of one hundred
millions of individuals and is considered as an agricultural pest and vector of parasites and diseases
(Lever 2005). According to Feare (1989) a downward trend has occurred in N European populations,
probably not due to usual fluctuations; in recent
times the global population was estimated as much as
more than 23,000,000 pairs, and underwent a moderate decline (>10%) in the northern countries, balanced by an increase in the southern ones (Feare
1989, BirdLife International 2004). The second
species is endemic to western Mediterranean; European populations represent >50% of global range.
Despite its limited distribution, European global population (> 2,100,000 pairs) has recently increased. S.
vulgaris was transferred from NonSPEC to SPEC3,
while S. unicolor status remained the same (NonSPECE = SPEC4) (Tucker and Heath 1994, BirdLife
International 2004). This is contradictory; the criterion used was mainly the recent trend, but the difference of natural history, population amount and range
distributions do not justify the discrepancy.
North African blue tit Parus teneriffae
Following Salzburger et al. (2002), Canary and N
African populations belong to a distinct species from
P. caeruleus. Europe holds a small population of the
subspecies ultramarinus on the isle of Pantelleria
(Sicilian Channel, Italy); it shows a very low productivity (Lo Valvo and Massa 1995), possibly balanced
by a limited winter mortality. According to criteria of
BirdLife International (2004) P. caeruleus is a NonSPECE; they do not treat P. teneriffae, but the unfa-
Massa imp.
25-11-2006
12:21
Pagina 11
Conservation and Mediterranean species
vorable status of this species not concentrated in
Europe should bring to the SPEC3 decision for it.
ENDEMIC BIRD AREAS
It is known that of the 127 bird species that became
extinct in the last 400 years, 116 (91 %) were island
species, which, therefore, disappeared at a rate 40
times faster than continental ones (Newton 2003). All
the taxa restricted only to some archipelagoes (e.g.:
Canary Is., Sardinia-Corsica, Balearic Is., Cyprus,
etc.) should be recorded within a separate list,
demanding attention at the highest level. Some birds,
indeed, cover a distribution that may be considered as
Endemic Bird Area (EBA), holding two or more
restricted range species (= with a range covering less
than 50,000 km2) (Long et al. 1996). Stattersfield et
al. (1998) already included Cyprus among EBA of the
world, giving to it a high priority; moreover, they listed Corsican mountains among secondary EBA (fewer
than two species are entirely confined to it), pointing
out that if Serinus citrinella corsicanus was recognized as a separate species, Corsica, Sardinia, Elba
and off-lying islands would be qualified as an EBA.
Afterwards, Sangster (2000), giving to Serinus corsicanus the species rank, proposed to include Corsica
among EBA. Actually, Sardinia, Corsica and Tuscany
Is., amounting to less than 35,000 km2, could be qualified as an EBA; nevertheless, following the Important Bird Areas global criteria (A level, category 2)
(Fishpool and Evans 2001), Balearic Islands, Sardinia, Corsica and Tuscany archipelago, amounting to
less than 50,000 km2 area, could be qualified as an
EBA, since they host the following taxa that have a
range covering less than 50,000 km2: Puffinus mauretanicus (Balearic Is.), Sylvia sarda (including balearica) (Balearic Is, Corsica, Sardinia, with a possible
extension to Pantelleria Is.), Sitta whiteheadi (Corsica), Serinus corsicanus (Sardinia, Corsica and Tuscany archipelago). Thus, the following species listed
as NonSPECE category (BirdLife International 2004)
show a concentration that should be used as a prerequisite to include them in the SPEC2 category.
Marmora’s warbler Sylvia sarda
It may be considered as an endemic taxon, very concentrated in few islands. According to Shirihai et al.
(2001) it is a superspecies comprising two insular
allospecies, S. balearica, endemic to Balearics, and
S. sarda, living in Corsica, Sardinia, Tuscany Is. and
Pantelleria Is. It is considered as secure, its overall
trend is unknown, and the whole population estimate
is very low (56-110,000 pairs, according to Tucker
and Heath 1994, 29-75,000 pairs according to
BirdLife International 2004); as the small population
of Pantelleria probably became extinct, the species is
eventually in decline. However, it is contradictory
that this local species falls within NonSPECE category, while the Dartford Warbler S. undata, with
1,900,000-3,700,00 pairs widespread over more than
1,000,000 km2, even if depleted and subjected to
large historical decline, lies in the SPEC2.
Cyprus warbler Sylvia melanothorax
Endemic only to Cyprus, formerly listed as SPEC2
(Tucker and Heath 1994), its global population, thanks
to a better estimate of previous figures, now amounts
to 70-140,000 pairs (BirdLife International 2004).
Cyprus wheatear Oenanthe cypriaca
Endemic to Cyprus, previously listed as SPEC2
(Tucker and Heath 1994), its global population,
according to a new by far larger estimate (90180,000 pairs: BirdLife International 2004), now is
considered out of danger. As the previous species, it
inhabits an EBA, covering less than 8,000 km2 (Stattersfield et al. 1998).
Citril finch Serinus [citrinella] corsicanus
Barbagli and Violani (1997) pointed out that the
adjective corsicanus should be adopted as the correct name instead of corsicana, agreeing in gender
with the generic name Serinus (masculine) and not
with the specific name citrinella, a feminine noun
placed in apposition. Pasquet and Thibault (1997)
considered distinctive ecology, vocalizations,
plumage pattern, measurements and genetic differences between corsicanus and citrinella within the
limit of subspecies/species; however, Sangster
(2000) reinterpreted their findings and considering
that there are strong evidences that both taxa have
unique evolutionary histories proposed corsicanus
as a valid species. The small and probably stable
11
Massa imp.
25-11-2006
12:21
Pagina 12
Massa
population of corsicanus (<85,000 pairs) (BirdLife
International 2004) is restricted only to Sardinia,
Corsica and Tuscany islands.
CONCLUSIONS
The list of bird species discussed above cannot be considered comprehensive. It emphasizes some emblematical examples, which allow highlighting the root
question requiring an imperative answer to achieve a
rational conservation strategy. It should take into
account species not only as systematic entities, but
also as biological ones, evolving and possibly composed by isolated populations, genetically shaped by
drift and selection. Other subspecies or evolutionary
significant entities would deserve more attention (e.g.:
Accipiter nisus wolterstorffi, Accipiter gentilis arrigonii from Corsica and Sardinia, Parus palustris siculus
from Sicily); recognition both of species and populations below the species level for assessment must be
guided by the general objective of preventing elements
of biodiversity from becoming extinct. The main conservation aim should be to preserve both evolutionary
processes and ecological viability of populations by
maintaining all the genetic populations within the
species so that the process of evolution would not be
excessively compelled. If there is substantial concern
that an isolated population of a species is on verge of
extinction, this information should be used to achieve
an official status enabling formal protection; following Alström and Mild (2004), the main advantage of
classifying all least-inclusive taxa (giving primacy to
evolutionary history) as species is that they receive
more attention, which can be crucial for endangered
taxa. The acknowledgement of conservation status for
isolated populations at risk of extinction is an action
taken in the process of using science in support of policy. Policy on endangered species conservation is
based on designation of extinction risk status for recognizably distinct biological entities; what is required
are biological units that may be designated on the
basis of their conservation status, not necessarily on
their taxonomical status, with the general objective of
preventing irreplaceable units of biodiversity from
becoming extinct.
Acknowledgements - I thank very much the members of
the executive board of the Centro Italiano Studi Ornitologici (Emiliano Arcamone, Fausto Barbagli, Giovanni
12
Boano, Pierandrea Brichetti, Lorenzo Fornasari, Fulvio
Fraticelli, Paolo Galeotti, Francesco Mezzavilla, Diego
Rubolini, Fernando Spina, Guido Tellini and Carlo
Violani) who commented constructively the manuscript,
sharing opinions here expressed; I also thank Toni Mingozzi and Nicola Baccetti who suggested fruitful comments on the first draft. Valentina Lo Verde and Daniela
Castellano improved the language.
REFERENCES
Alström P, Mild K 2004. ‘Biological’, ‘phylogenetic’ and
‘monophyletic’ species – same or different? Alula 10:
96-103.
Amadon D, Short LL 1992. Taxonomy of lower categories. Suggested guidelines. Pp. 11-38 in: Monk JF
(ed.), Avian Systematics and Taxonomy. Bulletin of
the British Ornithologists’ Club, centenary Vol. 112A.
Amengual JF, Gargallo G, Suarez M, Bonnin J, Gonzalez
JM, Rebassa M, McMinn M, 1999. The Mediterranean
Storm Petrel Hydrobates pelagicus melitensis at Cabrera archipelago (Balearic Islands, Spain): breeding,
moult, biometry and evaluation of the population size
by mark and recapture techniques. Ringing & Migration 19: 181-190.
Baillie JEM, Hilton-Taylor C, Stuart SN (eds) 2004. 2004
IUCN Red List of threatened Species. A global Species
Assessment. IUCN, Gland and Cambridge. 191 pp.
Barbagli F, Violani C 1997. Canaries in Tuscany. Bollettino del Museo regionale di Scienze naturali di Torino
15: 25-33.
Benkman CW 1987. Crossbill foraging behavior, bill
structure, and patterns of food profitability. Wilson
Bulletin 99: 351-368.
BirdLife International 2004. Birds in Europe. Population
estimates, trends and conservation status. BirdLife
International Ser. No. 12, Cambridge, UK (compilers:
Burfield I and van Bommel F).
Bretagnolle , 1992. Variation géographique des vocalisations de Pétrels ouest-paléarctiques et suggestions taxonomiques. Alauda 60: 251-252.
Bretagnolle V, Lequette B 1990. Structural variation in the
call of the Cory’s Shearwater (Calonectris diomedea,
Aves, Procellariidae). Ethology 85: 313-323.
Cagnon C, Lauga B, Hémery G, Mouchès C 2004. Phylogeographic differentiation of storm petrels (Hydrobates pelagicus) based on cytochrome b mithocondrial DNA variation. Marine Biology 145: 1257-1264.
Catalisano A, Lo Valvo F, Lo Verde G, Massa B 1988. Dati
biometrici sull’Uccello delle tempeste (Hydrobates
pelagicus). Atti IV Convegno italiano di Ornitologia,
Il Naturalista siciliano 12 (suppl.): 261-265.
Clouet M 2003. Taille du bec et période de reproduction
chez les Beccroisés des forets de pins. Revue d’Ecologie (Terre Vie) 58: 419-433.
Massa imp.
25-11-2006
12:21
Pagina 13
Conservation and Mediterranean species
Clouet M, Joachim J 1996. Premières élements de comparaison de trois populations françaises de Beccroisés
Loxia curvirostra. Alauda 64: 149-155.
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne
RK, 2000. Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution
17: 390-395.
de Queiroz K 1998. The general lineage concept of
species, species criteria, and the process of speciation.
A conceptual unification and terminological recommendations. Pp 57-75 in Howard DJ and Berlocher SH
(eds), Endless forms: species and speciation. Oxford
University Press, Oxford.
Eck S 1981. Reflexionen über die Taxonomie westpalaearktischer Loxia-Arten (Aves, Passeriformes,
Fringillidae). Zoologische Abhandlungen 37: 183-207
Fishpool LDC, Evans MI (eds.) 2001. Important Bird
Areas in Africa and associated islands: Priority sites
for conservation. Pisces Publ. & BirdLife International, Newbury & Cambridge.
Feare CJ 1989. The changing fortunes of an agricultural
bird pest: the European Starling. Agricultural Zoology
Reviews 3: 317-342.
Fraser DJ, Bernatchez L 2001. Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10: 2741-2752.
Green DM, 2005. Designatable units for status assessment
of endangered species. Conservation Biology 19:
1813-1820.
Groth JG 1993. Evolutionary differentiation in morphology, vocalizations, and allozymes among nomadic sibling species in the North American Red Crossbill
(Loxia curvirostra) complex. University of California
Publications Zoology 127: 1-143.
Hagemeijer WJM, Blair MJ (eds) 1997. The EBCC Atlas
of European Breeding Birds: their distribution and
abundance. T & AD Poyser, London. 903 pp.
Haring E, Riesing MJ, Pinsker W, Gamauf A 1999. Evolution of pseudo-control region in the mitochondrial
genome of Palearctic buzzards (genus Buteo). Journal
of Zoological Systematic and Evolution Research 37:
185-194.
Hazevoet CJ 1995. The Birds of the Cape Verde Islands.
British Ornithologists’ Union Check-list No. 13.
Heidrich P, Amengual J, Ristow D, Wink M 2000. Phylogenetic relationships among Procellariiformes based
on nucleotide sequences, with special consideration of
the Mediterranean and North Atlantic Shearwaters. Pp.
159-175 in: Yésou P and Sultana J (eds), Monitoring
and Conservation of Birds, Mammals and Sea Turtles
of the Mediterranean and Black Seas. Medmaravis and
BirdLife, Malta.
Helbig A 1994. Genetische Differenzierung von Möwen
und Sturmtauchern: ein Kommentar. Journal für
Ornithologie 135: 609-615.
Helbig AJ, Knox AG, Parkin DT, Sangster G, Collinson M
2002. Guidelines for assigning species rank. Ibis 144:
518-525.
Hemery G, D’Elbée E 1985. Discrimination morphologique des populations atlantique et méditerranéenne de Petrel tempete Hydrobates pelagicus. In:
Oiseaux marins nicheurs du Midi et de la Corse.
Annales du CROP 2: 63-67.
IUCN 2004. The 2004 IUCN Red List of threatened
species. www.redlist.org
Jouanin C, Roux F, Zino F 1977. Sur les premiers résultats
du baguage des Puffins cendrés Calonectris diomedea
aux îles Selvagens. Oiseau et Revue française d’Ornithologie 47: 351-358.
Kelt DA, Brown JH 2000. Species as units of analysis in
ecology and biogeography: are the blind leading the
blind? Global Ecology and Biogeography 9: 213-217.
Knox AG, 1990. The sympatric breeding of Common and
Scottish Crossbills Loxia curvirostra and L. scotica
and the evolution of crossbills. Ibis 132: 454-466.
Lalanne Y, Hémery G, Cagnon C, D’Amico F, D’Elbée J,
Mouchès C 2001. Discrimination morphologique des
sous-espèces d’Océanite tempête: nouveaux résultats
pour deux populations méditerranéennes. Alauda 69:
475-482.
Lavauden L 1924. Un caractère adaptatif du Bec croisé de
l’Afrique du Nord. Revue française d’Ornithologie 16:
301-302.
Lever C 2005. Naturalised birds of the world. T & AD
Poyser, London.
Long AJ, Crosby MJ, Stattersfield AJ, Wege DC 1996.
Towards a global map of biodiversity: patterns in the
distribution of restricted-range birds. Global Ecololy
and Biogeography 5: 281-304.
Lo Valvo F, Massa B 1995. Breeding performance of
Parus caeruleus ultramarinus on Pantelleria island
(Sicilian Channel). Rivista italiana di Ornitologia 65:
129-135.
Lo Valvo F, Massa B 2000. Some aspects of the population
structure of Storm Petrels Hydrobates pelagicus
breeding on a Mediterranean island. Ringing & Migration 20: 125-128.
Lo Valvo M, Massa B 1988. Considerations on a specimen
of Cory’s Shearwater ringed at Selvagem Grande and
recovered in the Central Mediterranean. Bocagiana
124: 1-5.
Lucchini V, Randi E 1998. Mitochondrial DNA sequence
variation and phylogeographical structure of rock partridge (Alectoris graeca) populations. Heredity 81:
528-536.
Massa B 1987. Variations in Mediterranean Crossbills
Loxia curvirostra. Bulletin of the British Ornithologists’ Club 107: 118-130.
Massa B, Lo Valvo M 1986. Biometrical and biological
considerations on the Cory’s Shearwater Calonectris
diomedea. Pp. 293-313 in: Mediterranean Marine Avifauna, Medmaravis & Monbailliu.
Massa B, Sultana J 1991. Status and conservation of the
Storm Petrel Hydrobates pelagicus in the Mediterranean. Il Merill 27: 1-5.
13
Massa imp.
25-11-2006
12:21
Pagina 14
Massa
Mc Neely JA, Miller KR, Reid WV, Mittermeier RA,
Werner TB 1990. Conserving the world’s biological
diversity. IUCN, Gland.
Newton I 2003.The speciation and biogeography of birds.
Academic Press, London.
O’Brien SJ, Mayr E 1991. Bureaucratic mischief: recognizing endangered species and subspecies. Science
251: 1187-1188.
Pasquet E, Thibault JC 1997. Genetic differences among
mainland and insular forms of the Citril Finch Serinus
citrinella. Ibis 139: 679-684.
Piertney SB, Summers R, Marquiss M 2001. Microsatellite
and mitochondrial DNA homogeneity among phenotypically diverse crossbill taxa in the UK. Proceedings
of the Royal Society of London B 268: 1511-1517.
Pimm SL, Jones HL, Diamond J 1988. On the risk of
extinction. American Naturalist 132: 757-785.
Questiau S, Gielly L, Clouet M, Taberlet P 1999. Phylogeographical evidence of gene flow among Common
Crossbill (Loxia curvirostra, Aves, Fringillidae) population at the continental level. Heredity 83: 196-205.
Randi E, Spina F, Massa B 1989. Genetic variability in
Cory’s Shearwater (Calonectris diomedea). Auk 106:
411-417.
Randi E, Tabarroni C, Rimondi S, Lucchini V, Sfougaris A
2003. Phylogeography of the Rock Partridge (Alectoris graeca). Molecular Ecology 12: 2201-2214.
Riddle BR, Hafner DJ 1999. Species as units of analysis in
ecology and biogeography: time to take the blinders
off. Global Ecology and Biogeography 8: 433-441.
Ristow D, Feldmann F, Scharlau W, Wink M 1990. Population structure, philopatry and mortality of Cory’
Shearwater Calonectris d. diomedea. Die Vogelwelt
111: 172-181.
Rojas M 1992. The species problem and conservation: what
are we protecting? Conservation Biology 6: 170-178.
Ryder OA 1986. Species conservation and systematics: the
dilemma of subspecies. Trends in Ecology and Evolution 1: 9-10.
Salzburger W, Martens J, Sturmbauer C 2002. Paraphyly
of the Blue Tit (Parus caeruleus) suggested from
cytochrome b sequences. Molecular and Phylogenetical Evolution 24: 19-25.
Sangster G 2000. Genetic distance as a test of species
boundaries in the Citril Finch Serinus citrinella: a critique and taxonomic reinterpretation. Ibis 142: 487-490.
Sangster G, Collinson JM, Helbig AJ, Knox AG, Parkin
DT 2005. Taxonomic recommendations for British
birds: third report. Ibis 147: 821-826.
Seibold I, Helbig AJ, Wink M 1993. Molecular Systematics of Falcons (Family Falconidae). Naturwissenchaften 80: 87-90.
Senar JC, Borras A, Cabrera T, Cabrera J 1993. Testing for
the relationship between coniferous crop stability and
Common Crossbill residence. Journal of field Ornithology 64: 464-469.
14
Shirihai H, Gargallo G, Helbig AJ 2001. Sylvia Warblers.
Identification, taxonomy and phylogeny of the genus
Sylvia. C Helm. ed., London.
Stattersfield AJ, Crosby MJ, Long AJ, Wege DC 1998.
Endemic Bird Areas of the World. Priorities for Biodiversity Conservation. BirdLife Conservation Series n°
7, BirdLife International ed., Cambridge.
Storey AE, Lien J 1985. Development of the first North
American colony of Manx Shearwaters. Auk 102:
395-401.
Swatschek I, Ristow D, Wink M 1994. Mate fidelity and
parentage in Cory’s shearwater Calonectris diomedea
– field studies and DNA fingerprinting. Molecular
Ecology 3: 259-262.
Thibault JC 1993. Natal philopatry in the Cory’s Shearwater (Calonectris d. diomedea) on Lavezzi Island, Corsica. Colonial Waterbirds 16 (1): 77-82.
Thibault JC 1994. Nest-site tenacity and mate fidelity in
relation to breeding success in Cory’s Shearwater
Calonectris diomedea. Bird Study 41: 25-28.
Thibault JC, Bretagnolle V 1998. A Mediterranean breeding colony of Cory’s Shearwater Calonectris
diomedea in which individuals show behavioural and
biometric characters of the Atlantic subspecies. Ibis
140: 523-528.
Tucker GM, Heath MF 1994. Birds in Europe: their conservation status. BirdLife International, Cambridge.
Tyrberg T 1991. Crossbill (Genus Loxia) evolution in the
West Palearctic - a look at the fossil evidence. Ornis
Svecica 1: 3-10.
Violani CG, Massa B 1993. Extinction of the Andalusian
Hemipode Turnix s. sylvatica (Desf.) in the Mediterranean region. Bulletin of the British Ornithologists’
Club 113: 225-229.
Wilson EO (ed) 1988. Biodiversity. National Academy
Press, Washington.
Wink M, Heidrich P, Kahl U, Swatschek I 1993. Inter- and
intraspecific variation of the nucleotide sequence of
the cytochrome b gene in Cory’s (Calonectris
diomedea), Manx Shearwater (Puffinus puffinus) and
the Fulmar (Fulmarus glacialis). Zeitschrift für Naturforschung 48c: 504-509.
Wink M, Döttlinger H, Nicholls MK, Sauer-Gürth H 1998.
Phylogenetic relationships between Black Shaheen
Falco peregrinus peregrinator, Red-naped Shaheen F.
pelegrinoides babylonicus and Peregrines F. peregrinus. Pp. 853-857 in: Chancellor RD and Meyburg BU (eds.), Raptors at risk. WWGBP, Berlin.
Wink M, Sauer-Gürth H 1998. Advances in the molecular
systematics of African raptors. Pp. 135-147 in: Chancellor RD and Meyburg B-U (eds.), Raptors at risk.
WWGBP, Berlin.
Wink M, Seibold I 1996. Molecular phylogeny of
Mediterranean Raptors (Families Accipitridae and Falconidae). Pp. 335-344 in: Muntaner J and Mayol J
(eds), Biology and Conservation of Mediterranean
Raptors. SEO, Madrid.